The Invasive Round Goby May Attach Its Eggs to Ships Or Boats

Aquatic Invasions (2017) Volume 12, Issue 2: 263–267 Open Access

Letter to the Editor

The invasive round goby may attach its eggs to ships or boats – but there is no evidence

Irene Adrian-Kalchhauser*, Anouk N’Guyen, Philipp E. Hirsch and Patricia Burkhardt-Holm University of Basel, Department of Environmental Sciences, Vesalgasse 1, CH-4055 Basel, Switzerland Author e-mails: [email protected] (IAK), [email protected] (AN), [email protected] (PEH), [email protected] (PBH) *Corresponding author

Received: 8 May 2017 / Accepted: 3 June 2017 / Published online: 7 June 2017 Handling editor: Kit Magellan

The round goby Neogobius melanostomus is an 2005; Adrian-Kalchhauser et al. 2016). Invasive gobies invasive vertebrate species that is currently on the have been observed close to boats, and they thrive in agenda of many environmental managers. In Europe, harbours (Vélez-Espino et al. 2010). Since invasive it is considered one of the “100 worst” invasive gobies accept artificial spawning substrates (Corkum species (Vilà et al. 2009). The species is reported to et al. 1998; Hirsch et al. 2016b), and goby eggs are alter the properties of aquatic ecosystems from able to withstand the harsh conditions expected contaminant recirculation to community restructuring during ship travel or boat transport (Rubinoff and to species extinctions (Hirsch et al. 2016a). Based on Rubinoff 1969; Hirsch et al. 2016b), it is possible that the common assumption that invasive goby eggs egg attachment plays a role in Ponto-Caspian goby could be translocated attached to ship or boat hulls translocations. Ballast water and bilge water (Janáč et al. 2012; Roche et al. 2015; Kotta et al. 2016), constitute additional possible vectors. Preventive hull cleaning approaches are increasingly being management approaches targeting boats and ships as considered as a preventive management option to vectors are therefore justified. Indirect support for a protect certain water bodies from round goby invasion. spread mode should suffice as an argument for To support a management initiative in Switzerland, preventive measures in the management of invasive we searched Web of Knowledge, Google Scholar, species. By definition such measures must be installed and PubMed for papers on round goby spread, round at the point of risk perception and before the risk has goby egg attachment, or round goby dispersal, and become real to such an extent that it can be screened them for mention of boats, ships, hulls, eggs, empirically tested. Nonetheless, the concept that or clutches. Russian publications were professionally Ponto-Caspian goby species attach their clutches to translated. We identified several scientific, peer- aquatic vessels is currently not supported by reviewed publications which report that the eggs of evidence and thus remains an untested hypothesis. invasive Ponto-Caspian goby species travel attached We therefore urge that the hypothesis should be to ship hulls, or which cite such reports. However, communicated as untested, and that evidence is we could not identify any evidence on the matter. presented if it exists. Ultimately, all reports were based on anecdotal reports, or on circumstantial evidence from goby behaviour Acknowledgements (Figure 1, Table 1). We agree with the commonly proposed assump- We are grateful to Anna Pevzner and Yulia Ivashchenko tion that invasive Ponto-Caspian goby species could for spotting relevant paragraphs in the Russian literature, which were then translated professionally, and to the be travelling with ships. Indirect evidence supports reviewers and the editor for their helpful comments and this assumption. Both spread patterns and population suggestions. genetics correlate with shipping routes (Wiesner

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Figure 1. Scientific literature containing statements on goby egg attachment to ship or boat hulls. See Table 1 for the associated statements from these papers.

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Table 1. Text passages from Figure 1.

It is now generally accepted that initial introductions have been through international shipping at major ports (Wiesner 2005) through accidental transport of juveniles/eggs in ballast water or as eggs Roche et al. 2015 attached to the ship’s hull (Ahnelt et al. 1998; Hayden and Miner 2009), followed by natural spreading from the point(s) of introduction (Roche et al. 2013).

Whichever route was taken, the round goby was probably introduced via ballast water released from Borcherding et al. ships (Ricciardi and Rasmussen 1998; Neilson and Stepien, 2009) or from eggs attached to ship hulls 2011 which in turn hatched at the new location (Ahnelt et al. 1998) and spread into nearby areas.

Hayden and Miner [discuss larval transport with ballast water] 2009

The transport of egg clutches of N. melanostomus and P. marmoratus on the hull of ships travelling along the Volga and its tributaries has recently been reported (Tsepkin et al. 1992; Sokolov et al. Ahnelt et al. 1998 1994b). A long incubation period (about two to three weeks) and the fact that freshly hatched N. melanostomus juveniles stay among the egg membranes for several additional days allow them to be moved considerable distances with a ship during that time (Moskal’kova 1996).

In light of the aforementioned characteristic of the round goby, the penetration of the sedentarian round goby from the Volga into the Moskva River by means of the passive dispersion of egg clutches attached to the fouling on the bottoms of barges travelling along the Volga and its tributaries Moskal’kova 1996 is probable, as suggested by several authors (Tsepkin et al. 1992; Sokolov et al. 1994a). Thus, if the Figure 1, left left 1, Figure eggs were laid during the mooring in the harbor, further moving by the ship provides conditions analogous to those provided by males when guarding the eggs. Ventilation of the clutch, its cleaning, and to some extent its protection from predation are provided during the boat motion.

At the same time, two new invading species were spotted for the first time in the Moscow river fish Sokolov et al. fauna – the round goby Neogobius melanostomus and the tubenose goby Preterorhinus marmoratus 1994a (Russian) – whose egg batches “swam up” from the Southern seas, apparently on the bottom of motor ships and barges, which were overgrown with coquina.

At that time, two new immigrant species were found for the first time in the Moscow River, the Sokolov et al. round goby, Neogobius melanostomus, and the tubenose goby, Proterorhinus marmoratus, whose 1994b eggs evidently were transported on the bottoms of boats and barges.

It is hard to believe that this slow-moving groundfish is capable of travelling several hundred kilometres against the stream, even surmounting cascades of dams, without assistance. In this case, Tsepkin et al. 1992 we are most likely dealing with passive settling, when batches of goby eggs are transported attached (Russian) to coquina growing on the bottom of motor ships and barges which go up the Volga and the Moscow canal.

In recent decades, this and other gobiid species have invaded new regions facilitated and accelerated by transport in the ballast water of ships, by transport of eggs on ships, by accidental stocking with Janáč et al. 2012 other fish species, by release of bait fish and through their ability to colonize riprap structures along inland waterways (Von Landwüst 2006).

In recent decades it showed a rapid expansion of its range, facilitated and accelerated by transport in the ballast water of ships (Ahnelt et al. 1998; Wonham et al. 2000), by transport of egg clutches on Von Landwüst ship hulls (Sokolov et al. 1994b), by accidental stocking together with other fish species (Friedl & 2006 Sampl 2000), release of bait fish (Prášek and Jurajda 2005), and through its ability to colonize riprap

Figure 1, center center 1, Figure structures along inland waterways (Jude 1996; Ahnelt et al. 1998).

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Table 1 (continued). Text passages from Figure 1.

The larvae and early juveniles of the round goby, similar to several demersal ﬁsh species, undergo diel vertical migration and therefore nocturnal ballasting can result in the transport of larval and Kotta et al. 2016 young round gobies (Hensler and Jude 2007; Hayden and Miner 2009). Moreover, the gobiidae are known to lay eggs on hulls or within sea-chests (Wonham et al. 2000; Jude et al. 1995) and their pelvic fins reduce maintenance costs while carried within ships' ballast water (French and Jude 2001).

The invasive success of gobies and blennies may be explained in part by their crevicolous nature: both groups seek refuge and lay eggs in small holes, and may take advantage of the ballast-intake Wonham et al. holes on ship hulls. [...] The crevicolous nature of gobies when seeking refuge and laying eggs may 2000 predispose them to ballast-water transport, particularly if the ballast-intake grates on ship hulls present appealing crevices (Carlton 1985; Hoese 1973; Springer and Gomon 1975).

In this case spawning occurred on the upper surfaces of a hollowed out oak log. One round goby was observed guarding eggs in a beer can on the bottom of the St. Clair River in June (K. Johnson and Jude et al. 1995 Greg Lashbrook, personal communication, Clyde, MI), and we collected newly hatched larval round gobies from Lake St. Clair Chara beds, where spawning presumably occurred.

Herdman, Thompson and Scott (1897) described the composition of plankton samples pumped aboard a steamer into a deck tank as the vessel crossed the north Atlantic Ocean. Taxa passing through the pumps into and through the ship's seawater system included numerous species of protists (diatoms, dinoflagellates, radiolarians, foraminiferans), and of adult and larval animals (hydromedusae, polychaetes, cladocerans, ostracods, barnacle cyprids, harpacticoid, cyclopoid and calanoid copepods, hyperiid amphipods, mysids, isopods, shrimp and crab larvae, euphausiids, Carlton 1985 bivalve and gastropod larvae, pteropods, chaetognaths, and fish the last including eggs, embryos, and Figure 1, right 1, Figure larvae). Of the remaining "possible" cases, four species of blennies and gobies may have been transported either on or in vessel fouling or in ballast water. McCosker and Dawson (1975) have demonstrated that Lupinoblennius, Hypleurochilus, and Lophogobius are all euryhaline and could survive transport through the freshwater sections of the Canal, while Rubinoff and Rubinoff (1969) experimentally determined that the eggs of the stenohaline, Gobiosoma, can survive in freshwater portions of the Canal and still remain viable.

Brittan et al. (1963) have suggested that the eggs [of Acanthogobius flavimanus and Tridentiger trigonocephalus] may have been transported attached to fouling organisms in the sea water system. Hoese 1973 Acanthogobius flavimanus lays eggs in burrows constructed in mud, while Tridentiger deposits its eggs on oyster shells. Acanthogobius is known to lay eggs in earthen pipes and might conceivably spawn in sea water intake pipes or in a sheltered space under the hull of a ship.

Newman (1963, pp. 128-9) feels Palaemon larvae may have been carried in a ship 's sea water Brittan et al. 1963 system which was partially clogged with fouling organisms, such as tubeworms and barnacles. A. flavimanus could have been introduced in a similar manner.

Springer and Dutt and Visveswara Rao (1961) reported O. zebra (as Petroscirtes bipunctata) nesting in holes in Gomon 1975 mangrove stems in the Godavari River estuary (16º28′N, 82º03′E) in India.

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